Background:
The most prevalent consequence of diabetes mellitus is diabetic foot infections (DFIs). Prior to the final treatment established by the culture findings, the early identification of infections may be used as a prescription for an empirical therapy. This study examines the microbiological profile and antimicrobial susceptibility profile of the bacteria that cause DFI.
Methods:
This research aims to determine the culture and sensitivity trend of aerobic bacterial isolates of DFI in Asian nations over a 5-year period. The article was searched using PubMed and Google Scholar with the keywords ‘Diabetic Foot Infections’, ‘Antibiotic’, ‘Microbiological Profile’, and their combinations. The author uses publications from 2018 to 2022 in Indonesian and English to select the appropriate journal.
Results:
The author identified 11 relevant articles with microbiological profiles and sensitivity patterns in DFI. A total of 3097 isolates were found in 2498 patients with DFI. Gram-negative bacteria were the leading source of infection (n=1737; 56%). Totally, 1148 (or 37%) of all isolates were aerobic Gram-positive cocci. Staphylococcus aureus was the most commonly isolated aerobe (n=608, 20%), followed by Pseudomonas aeruginosa (n=451, 15%). Gram-positive bacteria showed good susceptibility to trimethoprim-sulfamethoxazole, chloramphenicol, doxycycline, vancomycin, and linezolid. Gram-negative bacteria displayed excellent susceptibility to aminoglycosides, piperacillin-tazobactam, and carbapenems.
Conclusions:
Gram-negative microorganisms were the most prevalent cause of DFI. This study’s findings will facilitate the development of future empirical therapeutic guidelines for the treatment of DFI.
Keywords: antibiotic, diabetic foot infection, microbiological profile
Highlights
Diabetic foot infections (DFIs) are the most prevalent complication among diabetes mellitus patients.
Gram-negative bacteria were the leading cause of DFIs.
Culture and sensitivity patterns of bacteria are required for future DFI therapy.
Background
Diabetic foot infections (DFIs) are the most common complication of diabetes. Soft tissue infections or osteomyelitis are the two types of infections that could arise. The International Working Group on the Diabetic Foot (IWGDF) and the Infectious Diseases Society of America (IDSA) adopt the following grading system: grade 1 (uninfected), grade 2 (mild infection), grade 3 (moderate infection), and grade 4 (severe infection)1–4.
Gram-positive bacteria, such as Staphylococcus aureus, Streptococcus pyogenes, and Enterococcus spp., and Gram-negative rods, such as Enterobacter spp., Pseudomonas aeruginosa, and Pseudomonas fluorescens, are the most frequent microorganisms responsible for DFI1–13.
The first management and therapy for DFI is empiric antibiotic therapy, depending on the pattern of antibiotic sensitivity of the infection, followed by wound care and surgery. In addition to a variety of other considerations, empiric treatment should be based on the clinician’s best estimate of the likely causative bacteria and their local antibiotic susceptibilities (e.g. drug allergies, recent hospitalization, patient co-morbidities, the likelihood of adverse events or potential drug interactions, and the availability and cost of various agents). This research aims to determine the culture and sensitivity trend of aerobic bacterial isolates of DFI in Asian nations over a 5-year period. A literature study is necessary to examine the microbiological profile and antibiotic susceptibility pattern of the bacteria causing DFI2.
Methods
The following strategy was used terms on Google Scholar and PubMed search engine was ‘diabetic foot infections’, ‘antibiotic’, ‘microbiological Profile’, and its combination. After searching those keywords, the author uses publications from 2018 to 2022 in Indonesian and English to select the appropriate journal. Journals were reviewed based in the title and abstract and followed inclusion criteria. The inclusion criteria were studied on patients with DFI, and microbiological cultures and sensitivity tests were performed. The journal search strategy is shown in Figure 1. This research aims to identify the culture and sensitivity trend of aerobic bacterial isolates from DFI in Asian nations over a 5-year period.
Figure 1.
Flow diagram of the search strategy.
Results and discussions
The author identified 11 relevant articles with a microbiological profile and sensitivity pattern in DFI (Table 1). All of the studies come from Asian countries: three studies from Indonesia, two studies from India, one study from Malaysia, two studies from China, one study from Oman, one study from Turkey, and one study from Iran. Five studies classified patients according to IDSA/IWGDF, or Wagner, and six studies did not classify patients.
Table 1.
Summary of the relevant article
| Author | Isolates | Antibiotics |
|---|---|---|
| Sekhar et al. 1 | 1. Staphylococcus aureus | 1. Doxicycline |
| 2. Pseudomonas aeruginosa | 2. Meropenem | |
| Wu et al. 10 | 1. Staphylococcus aureus | 1. Vancomycin, Linezolid |
| 2. Pseudomonas aeruginosa | 2. Fluoroquinolone, Aminoglycoside Carbapenem | |
| Li et al. 9 | 1. Staphylococcus aureus | 1. Vancomycin, Linezolid, Piperacillin-tazobactam |
| 2. Pseudomonas aeruginosa | 2. Carbapenem, Aminoglycoside | |
| Rahmawati et al. 4 | 1. Enterococcus faecalis | 1. Vancomycin, Ampicillin Sulbactam |
| 2. Klebsiella pneumoniae | 2. Meropenem | |
| Donastin et al. 3 | 1. Staphylococcus aureus | Carbapenem |
| 2. Klebsiella pneumoniae | ||
| Ahmadishooli et al. 5 | 1. Escherichia coli | 1. Vancomycin |
| 2. Enterococcus spp. | 2. Meropenem, Ciprofoxacin | |
| Goh et al. 11 | 1. Staphylococcus aureus | 1. Vancomycin |
| 2. Pseudomonas aeruginosa | 2. Meropenem, Amikacin | |
| Salim et al. 12 | 1. Staphylococcus aureus | 1. Vancomycin, Tigecycline, Linezolid |
| 2. Klebsiella pneumoniae | 2. Carbapenem | |
| Sannathimma et al. 14 | 1. Staphylococcus aureus | 1. Doxicycline, TMP-SMX, Vancomycin, Linezolid |
| 2. Pseudomonas aeruginosa | 2. Carbapenem, Aminoglycoside | |
| Degloorkan et al. 8 | 1. Staphylococcus aureus | 1. Rifampicin, Cefoperazone, Tigecycline |
| 2. Morganella morganii, Proteus mirabilis | 2. Fluoroquinolone, Carbapenem | |
| Aydin et al. 7 | 1. Staphylococcus aureus | 1. Vancomycin, Teicoplanin, Linezolid, TMP-SMX |
| 2. Klebsiella pneumoniae | 2. Meropenem, Amikacin, Piperacillin-tazobactam |
A total of 3097 isolates were found in 2498 patients with DFI. Gram-negative bacteria were the leading source of infection (n=1737; 56%). Totally, 1148 (or 37%) of all isolates were aerobic Gram-positive cocci. S. aureus, however, was the most frequently isolated aerobe (n=608; 19.6%), followed by P. aeruginosa (n=451; 14.5%) (Fig. 2).
Figure 2.
Proportion and frequency of bacterial isolated from diabetic foot infection patients.
S. aureus, a Gram-positive bacterium (Fig. 3), exhibited high susceptibility to oxacillin (100%), chloramphenicol (100%), teicoplanin (100%), vancomycin (100%), tigecycline (100%), and linezolid (100%), and good susceptibility to trimethoprim/sulfamethoxazole (87%), gentamycin (84%), clindamycin (78%), and doxycycline (74%).
Figure 3.
Antibiotic sensitivity patterns of aerobic gram-positive and negative isolates.
While methicillin-resistant S. aureus showed high-level susceptibility to linezolid (100%), tigecycline (100%) and doxycycline (100%), vancomycin (93%), and trimethoprim/sulfamethoxazole (83%). On the other hand, group B Streptococcus and Enterococcus spp. showed high susceptibility to chloramphenicol (100%), teicoplanin (100%), doxycycline (100%), gentamycin (99%), linezolid (90–95%), tigecycline (80–100%), and vancomycin (96%). Multiple global studies have documented a rise in S. aureus and Enterococcus faecalis vancomycin resistance. In order to prevent the future emergence of vancomycin-resistant strains, the prudent use of these medications is strongly recommended. In this investigation, we found that trimethoprim-sulfamethoxazole, chloramphenicol, and doxycycline are suitable for the empirical treatment of Gram-positive isolates6.
Gram-negative bacteria demonstrated excellent susceptibility to imipenem (84–94%), meropenem (61–99%), piperacillin-tazobactam (63–88%), and amikacin (50–86%). Carbapenems, cephalosporins, aminoglycosides, piperacillin/tazobactam, and fluoroquinolone have shown high-level susceptibility to P. aeruginosa. The similar good susceptibility of these treatments has been documented by numerous studies6. The high rate of susceptibility may be attributable to the restricted use of these drugs due to their expensive cost, increased risk of adverse effects, and stringent usage restrictions. Enterobacteriaceae and Acinetobacter baumannii showed low-level susceptibility to cephalosporins. This is due to the widespread use of these medications for treatment and prevention as well as the creation of resistant strains. Compared to Gram-positive organisms, Gram-negative organisms are known to develop resistance to several antibiotics more quickly. These results indicate that aminoglycosides, piperacillin-tazobactam, and carbapenems are suitable for the empirical treatment of Gram-negative bacterial infections in DFI.
Conclusions
Gram-negative bacteria were the most common cause of DFI. We have shown that trimethoprim-sulfamethoxazole and doxycycline are suitable for the empirical treatment of Gram-positive bacterial infections, while aminoglycosides and carbapenems are suitable for Gram-negative bacterial infections in DFI.
Ethical approval
This study does not need ethical review.
Consent
This study does not need inform consent.
Sources of funding
This study did not receive any specific grant from funding agencies, commercial, or not-forprofit sectors.
Conflicts of interest disclosure
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Author contribution
T.E.C.J.H.: conceptualization, writing original draft preparation, supervision, validation. I.R.: writing the paper and editing, data interpretation, data collecting, validation. Y.M.L.: writing the paper and editing, data interpretation, validation, visualization. D.R.: writing the paper and editing, data interpretation, validation, visualization. P.S.: writing the paper and editing, methodology, data interpretation. S.A.: writing the paper and editing, supervision, validation.
Research registration unique identifying number (UIN)
1. Name of the registry: NA.
2. Unique Identifying number or registration ID: NA.
3. Hyperlink to your specific registration (must be publicly accessible and will be checked): NA.
Guarantor
Irene Ratridewi, Department of Pediatrics, Faculty of Medicine, Universitas Brawijaya – Dr. Saiful Anwar General Hospital, Jl. Jaksa Agung Suprapto No. 2, Klojen, Malang 65112, East Java, Indonesia. E-mail address: irene24.fk@ub.ac.id
Provenance and peer review
Not commissioned, externally peer-reviewed.
Acknowledgments
The authors thank the support of parents, family, and friends for making this research paper possible.
Footnotes
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
Published online 17 February 2023
Contributor Information
Thomas E.C.J. Huwae, Email: huwaethomas@ub.ac.id.
Irene Ratridewi, Email: irene24.fk@ub.ac.id.
Yulanda M. Lena, Email: yulanda89@student.ub.ac.id.
Dewi Retnoningsih, Email: dewiretnoningsih29@gmail.com.
Panji Sananta, Email: panjisananta@ub.ac.id.
Syaifullah Asmiragani, Email: syaifullahag@ub.ac.id.
References
- 1. Sekhar MS, Unnikrishnan MK, Rodrigues GS, et al. Antimicrobial susceptibility pattern of aerobes in diabetic foot ulcers in a South-Indian tertiary care hospital. Foot 2018;37(June):95–100. [DOI] [PubMed] [Google Scholar]
- 2. Lipsky BA, Senneville É, Abbas ZG, et al. Guidelines on the diagnosis and treatment of foot infection in persons with diabetes (IWGDF 2019 update). Diabetes Metab Res Rev 2020;36(S1):1–24. [DOI] [PubMed] [Google Scholar]
- 3. Donastin A, Aisyah A. Microbial pattern of diabetic foot ulcer patient in Jemursari Islamic Hospital Surabaya Period 2012-2016. Indones J Med Lab Sci Technol 2019;1:22–32. [Google Scholar]
- 4. Rahmawati M, Maulidya V, Ramadhan AM. Kajian Kesesuaian Pemilihan Antibiotik Empiris pada Pasien Ulkus Diabetikum Di Instalasi Rawat Inap Rumah Sakit Abdul Wahab Sjahranie Samarinda. Proceeding of Mulawarman Pharmaceuticals Conferences. 8 November 2018: 119–27.
- 5. Ahmadishooli A, Davoodian P, Shoja S, et al. Frequency and antimicrobial susceptibility patterns of diabetic foot infection of patients from Bandar Abbas District, Southern Iran. J Pathog 2020;2020:1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Mohebi S, Parham M, Sharifirad G, et al. Relationship between Perceived Social support and self‑care behavior in Type 2 Diabetics: a Cross-sectional study. J Educ Health Promot 2018;7:48. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Aydin O, Celik A. Evaluation of microbiological profiles of diabetic foot infections at a tertiary hospital. Cerrahpasa Med J 2022;46:44–49. [Google Scholar]
- 8. Degloorkar S, Shah BC, Patel K. Culture and sensitivity pattern of aerobic bacterial isolates in diabetic foot infections, in a suburban tertiary care hospital in Mumbai. Int Surg J 2021;8:3046. [Google Scholar]
- 9. Li X, Qi X, Yuan G, et al. Microbiological profile and clinical characteristics of diabetic foot infection in Northern China: a retrospective multicentre survey in the Beijing area. J Med Microbiol 2018;67:160–8. [DOI] [PubMed] [Google Scholar]
- 10. Wu M, Pan H, Leng W, et al. Distribution of microbes and drug susceptibility in patients with diabetic foot infections in Southwest China. J Diabetes Res 2018;2018:9817308. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Goh TC, Bajuri MY, Nadarajah SC, et al. Clinical and bacteriological profile of diabetic foot infections in a tertiary care. J Foot Ankle Res 2020;13:1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Salim SE, Sukrama IDM, Fatmawati NND, et al. Bacterial Patterns in Diabetic Foot Patients and Their Resistance to Antibiotics at the Sanglah Central General Hospital for the Period January 1st 2017 until February 28th 2018. J Med Udayana 2020;9:98–104. [Google Scholar]
- 13. Del Core MA, Ahn J, Lewis RB, et al. The evaluation and treatment of diabetic foot ulcers and diabetic foot infections. Foot Ankle Orthop 2018;3:247301141878886. [Google Scholar]
- 14. Sannathimmappa MB, Nambiar V, Aravindakshan R, et al. Diabetic foot infections: Profile and antibiotic susceptibility patterns of bacterial isolates in a tertiary care hospital of Oman. J Educ Health Promot 2021;10:254. [DOI] [PMC free article] [PubMed] [Google Scholar]